Sexual Reproduction and Seasonality of the Alaskan Red Tree Coral, Primnoa pacifica Rhian G. Waller1*, Robert P. Stone2, Julia Johnstone3, Jennifer Mondragon4 1 University of Maine, School of Marine Sciences, Darling Marine Center, Walpole, Maine, United States of America, 2 Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Juneau, Alaska, United States of America, 3 University of Maine, Darling Marine Center, Walpole, Maine, United States of America, 4 Alaska Regional Office, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Juneau, Alaska, United States of America Abstract The red tree coral Primnoa pacifica is an important habitat forming octocoral in North Pacific waters. Given the prominence of this species in shelf and upper slope areas of the Gulf of Alaska where fishing disturbance can be high, it may be able to sustain healthy populations through adaptive reproductive processes. This study was designed to test this hypothesis, examining reproductive mode, seasonality and fecundity in both undamaged and simulated damaged colonies over the course of 16 months using a deepwater-emerged population in Tracy Arm Fjord. Females within the population developed asynchronously, though males showed trends of synchronicity, with production of immature spermatocysts heightened in December/January and maturation of gametes in the fall months. Periodicity of individuals varied from a single year reproductive event to some individuals taking more than the 16 months sampled to produce viable gametes. Multiple stages of gametes occurred in polyps of the same colony during most sampling periods. Mean oocyte size ranged from 50 to 200 mm in any season, and maximum oocyte size (802 mm) suggests a lecithotrophic larva. No brooding larvae were found during this study, though unfertilized oocytes were found adhered to the outside of polyps, where they are presumably fertilized. This species demonstrated size-dependent reproduction, with gametes first forming in colonies over 42-cm length, and steady oocyte sizes being achieved after reaching 80-cm in length. The average fecundity was 86 (612) total oocytes per polyp, and 17 (612) potential per polyp fecundity. Sub-lethal injury by removing 21–40% of colony tissue had no significant reproductive response in males or females over the course of this study, except for a corresponding loss in overall colony fecundity. The reproductive patterns and long gamete generation times observed in this study indicate that recruitment events are likely to be highly sporadic in this species increasing its vulnerability to anthropogenic disturbances. Citation: Waller RG, Stone RP, Johnstone J, Mondragon J (2014) Sexual Reproduction and Seasonality of the Alaskan Red Tree Coral, Primnoa pacifica. PLoS ONE 9(4): e90893. doi:10.1371/journal.pone.0090893 Editor: John Murray Roberts, Heriot-Watt University, United Kingdom Received October 11, 2013; Accepted February 6, 2014; Published April 25, 2014 This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Funding: This work was funded by the National Oceanic and Atmospheric Administration Alaska Fisheries Science Center, and through the National Geographic Society. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction otherwise we know very little that will assist us in gauging their capability to recover from disturbance. Data on the reproductive Primnoidae is one of the most dominant gorgonian families in processes of cold-water corals is still in its infancy compared to the deep-sea and polar regions, with 233 valid species known to date wealth of data available for their shallow water zooxanthellate [1]. Primnoids are found in all ocean basins and are most counterparts [10,9,11]. Advances in this discipline are largely numerous in Antarctic waters where the family is thought to have hampered by inability to sample specimens at regular intervals in originated [1]. This family is primarily deep-sea, with most current most deep-sea environments. records coming from slope and abyssal depths whereas shallow Recent submersible observations in the eastern Gulf of Alaska populations are rare. The genus Primnoa is only found in the North shelf habitats clearly indicate that red tree corals are highly Pacific, North Atlantic and subantarctic South Pacific regions, vulnerable to disturbance from fishing gear and that a much with the red tree coral, Primnoa pacifica Kinoshita, 1907, known higher proportion of large colonies are damaged compared to only from North Pacific waters [2]. This species can attain massive smaller colonies. Some cold-water corals subjected to mechanical size (up to 5 m in height and 7 m in width; 3, R. Stone, personal disturbance exhibit reduced reproductive fitness (i.e. fecundity) via observations) and form vast monospecific thickets that provide resource re-allocation and planulae expulsion [12,13]. Further- habitat for fish [3,4] and invertebrates [5]. more, larger, more susceptible, colonies are thought to be Growth rates show that P. pacifica is a slow growing coral [6,7] considerably more fecund than smaller colonies [14]. Both of and there is an indication that successful recruitment events occur these factors may influence the ability of habitats dominated by on a decadal scale (Stone pers obs). Many cold-water gorgonians red tree corals to recover from fishing gear disturbance. appear to be gonochoristic (i.e. separate sexes at the colony level) Shallow-water habitats in several high-latitude fjords sustain brooders that likely have seasonal reproductive cycles [8,9] but benthic communities that are similar to those usually found in PLOS ONE | www.plosone.org 1 April 2014 | Volume 9 | Issue 4 | e90893 Red Tree Coral Reproduction much deeper water. The term ‘‘deepwater emergence’’ has been Sample Collection used to describe this phenomenon, though the environmental Thirty-eight healthy (i.e. undamaged) colonies (42 to 162 cm factors that allow these species to survive much shallower than total length along the longest axis) were haphazardly selected for their usual distribution (often by thousands of meters) are not yet tagging between 8th and 10th September 2010. Colonies were fully understood. Shallow-water temperatures in these fjords tend tagged above the holdfast with numbered, plastic cinch-type tags to be much cooler mimicking temperatures usually found at by scuba divers. The depth range for all tagged colonies was 9.8 to bathyal depths [15,16]. Nutrient-rich upwelling, strong current 17.1 m mean lower low water (all depths reported hereafter are regimes, temperatures at the surface layers being equal to the deep referenced to mean lower low water). Reference images were ocean and reduced light levels are other factors that could collected of each colony with a meter stick scale, and Image J influence how these deep-sea species survive shallower than their (National Institutes of Health) was used to calculate flat-plane area normal distributions [7,16]. Several shallow systems worldwide of colonies. that support deepwater emerged coral species have been Samples were collected from all 38 tagged-colonies during six documented – Chile [17], Norway [18], New Zealand time periods over an 18-month span: September 2010, December [19,20,21], Alaska [7] and British Columbia [22]. The coral 2010, March 2011, June 2011, and January 2012. In September species that appear in these fjord systems are often ecosystem 2011, extremely poor visibility limited us to collected samples from engineers (in sensu [23]), altering both the local benthic and only 10 colonies (9 females and 1 male). The poor water visibility physical environment and providing suitable microhabitat for was due to heavy sediment loading and corresponded with warm colonization of many associated species [24]. These shallow-water air temperatures and the onset of the rainy season in the region— communities appear to mimic those of the deep sea and thus both factors increasing stream run-off and glacial melt. provide a unique opportunity to use the easily accessible habitats Pieces approximately 4–7 cm in length (containing ,30 polyps) as ‘‘living laboratories’’ to study the physiological processes of were carefully sampled from a distal branch of each tagged colony. deep-sea organisms. Samples were isolated in individual jars in situ and returned to the A recently discovered shallow-water population of red tree surface where they were kept in containers of cold seawater until corals in Tracy Arm, Holkham Bay, Southeast Alaska provided an onboard processing. The number of polyps per 1 cm was counted unprecedented opportunity to collect reproductive tissue samples for each sample collected, averaging over a 5 cm span of skeleton. at regular intervals year-round from the same colonies. Red tree Ten of the 38 colonies were randomly selected following the corals exhibit keystone species characteristics in Gulf of Alaska initial sampling (September 2010) for the simulated physical habitats where it provides refuge habitat for at least 12 species of damage treatment group.